Age-related structural-mechanical property changes in human peroneus longus muscle
Abstract
Background: Functional impairment of the muscle-tendon unit is one of the most remarkable effects of aging. The function of the peroneus longus muscle is to stabilise the foot and ankle joint. A deterioration of the structural and mechanical properties of this muscle can potentially lead to foot problems in older adults. This study aimed to investigate the effects of age on structural, histological, and mechanical features in peroneus longus muscle samples taken from embalmed cadavers of two different age groups; young adult (30–60 years) and old adult (over 60 years).
Materials and methods: The mechanical property was analysed through the results of cross-sectional area, tensile, tensile stress, and modulus of elasticity. The arran- gement of the collagen in the perimysium and tendon was examined by scanning electron microscopy. Fatty infiltration within the musculotendinous junction was evaluated by Masson’ trichrome stained muscle sections.
Results: This study thus provides evidence that there are indeed age-induced mechanical property changes in the peroneus longus muscle, which include reductions in the tensile force, tensile stress, and modulus of elasticity, and is related to the malformation of collagen fibrils and the massive fat accumulation in the musculotendinous junction.
Conclusions: These alterations may further result in a reduction of muscle strength and quality in an older person.
Keywords: agingcollagenmusculotendinous junctiontendon
References
- Avery NC, Bailey AJ. Enzymic and non-enzymic cross-linking mechanisms in relation to turnover of collagen: relevance to aging and exercise. Scand J Med Sci Sports. 2005; 15(4): 231–240.
- Brandes CB, Smith RW. Characterization of patients with primary peroneus longus tendinopathy: a review of twenty-two cases. Foot Ankle Int. 2000; 21(6): 462–468.
- Bubra PS, Keighley G, Rateesh S, et al. Posterior tibial tendon dysfunction: an overlooked cause of foot deformity. J Family Med Prim Care. 2015; 4(1): 26–29.
- Couppé C, Hansen P, Kongsgaard M, et al. Mechanical properties and collagen cross-linking of the patellar tendon in old and young men. J Appl Physiol (1985). 2009; 107(3): 880–886.
- Dudhia J, Scott CM, Draper ERC, et al. Aging enhances a mechanically-induced reduction in tendon strength by an active process involving matrix metalloproteinase activity. Aging Cell. 2007; 6(4): 547–556.
- Grimby G, Danneskiold-Samsøe B, Hvid K, et al. Morphology and enzymatic capacity in arm and leg muscles in 78-81 year old men and women. Acta Physiol Scand. 1982; 115(1): 125–134.
- Hepple RT, Ross KD, Rempfer AB. Fiber atrophy and hypertrophy in skeletal muscles of late middle-aged Fischer 344 x Brown Norway F1-hybrid rats. J Gerontol A Biol Sci Med Sci. 2004; 59(2): 108–117.
- Hughes VA, Roubenoff R, Wood M, et al. Anthropometric assessment of 10-y changes in body composition in the elderly. Am J Clin Nutr. 2004; 80(2): 475–482.
- Kano Y, Shimegi S, Furukawa H, et al. Effects of aging on capillary number and luminal size in rat soleus and plantaris muscles. J Gerontol A Biol Sci Med Sci. 2002; 57(12): B422–B427.
- Keller K, Engelhardt M. Strength and muscle mass loss with aging process. Age and strength loss. Muscles Ligaments Tendons J. 2013; 3(4): 346–350.
- Kitaoka HB, Luo ZP, An KN. Effect of the posterior tibial tendon on the arch of the foot during simulated weightbearing: biomechanical analysis. Foot Ankle Int. 1997; 18(1): 43–46.
- Kjaer M. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev. 2004; 84(2): 649–698.
- Kohls-Gatzoulis J, Angel JC, Singh D, et al. Tibialis posterior dysfunction: a common and treatable cause of adult acquired flatfoot. BMJ. 2004; 329(7478): 1328–1333.
- Kokubo T, Hashimoto T, Nagura T, et al. Effect of the posterior tibial and peroneal longus on the mechanical properties of the foot arch. Foot Ankle Int. 2012; 33(4): 320–325.
- Kolovou G, Katsiki N, Pavlidis A, et al. Ageing mechanisms and associated lipid changes. Curr Vasc Pharmacol. 2014; 12(5): 682–689.
- Kurose T, Asai Y, Mori E, et al. Distribution and change of collagen types I and III and elastin in developing leg muscle in rat. Hiroshima J Med Sci. 2006; 55(3): 85–91.
- Lecker SH, Goldberg AL, Mitch WE. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J Am Soc Nephrol. 2006; 17(7): 1807–1819.
- Lexell J, Taylor CC. Variability in muscle fibre areas in whole human quadriceps muscle: effects of increasing age. J Anat. 1991; 174: 239–249.
- Louwerens JW, van Linge B, de Klerk LW, et al. Peroneus longus and tibialis anterior muscle activity in the stance phase. A quantified electromyographic study of 10 controls and 25 patients with chronic ankle instability. Acta Orthop Scand. 1995; 66(6): 517–523.
- Lui TH, Hau WW. Peroneus longus tendoscopy at the sole. Arthrosc Tech. 2018; 7(5): e479–e483.
- Lui TH. Stabilization of medial longitudinal foot arch by peroneus longus transfer. Foot (Edinb). 2016; 27: 22–26.
- Marcus RL, Addison O, Kidde JP, et al. Skeletal muscle fat infiltration: impact of age, inactivity, and exercise. J Nutr Health Aging. 2010; 14(5): 362–366.
- Mendicino RW, Orsini RC, Whitman SE, et al. Fibular groove deepening for recurrent peroneal subluxation. J Foot Ankle Surg. 2001; 40(4): 252–263.
- Menz HB. Biomechanics of the Ageing Foot and Ankle: A Mini-Review. Gerontology. 2015; 61(4): 381–388.
- Mizel MS, Temple HT, Scranton PE, et al. Role of the peroneal tendons in the production of the deformed foot with posterior tibial tendon deficiency. Foot Ankle Int. 1999; 20(5): 285–289.
- Narici MV, Maganaris CN, Reeves ND, et al. Effect of aging on human muscle architecture. J Appl Physiol (1985). 2003; 95(6): 2229–2234.
- Narici MV, Maganaris CN. Plasticity of the muscle-tendon complex with disuse and aging. Exerc Sport Sci Rev. 2007; 35(3): 126–134.
- Onambele GL, Narici MV, Maganaris CN. Calf muscle-tendon properties and postural balance in old age. J Appl Physiol (1985). 2006; 100(6): 2048–2056.
- Perera AM, Mason L, Stephens MM. The pathogenesis of hallux valgus. J Bone Joint Surg Am. 2011; 93(17): 1650–1661.
- Ruggiero M, Cless D, Infantolino B. Upper and Lower Limb Muscle Architecture of a 104 Year-Old Cadaver. PLoS One. 2016; 11(12): e0162963.
- Seah NE, de Magalhaes Filho CD, Petrashen AP, et al. Autophagy-mediated longevity is modulated by lipoprotein biogenesis. Autophagy. 2016; 12(2): 261–272.
- Ugbolue UC, Gislason MK, Carter M, et al. Tensile properties of the transverse carpal ligament and carpal tunnel complex. Clin Biomech (Bristol, Avon). 2015; 30(7): 649–656.
- van Haaren EH, van der Zwaard BC, van der Veen AJ, et al. Effect of long-term preservation on the mechanical properties of cortical bone in goats. Acta Orthop. 2008; 79(5): 708–716.
- Watanabe K, Kitaoka HB, Fujii T, et al. Posterior tibial tendon dysfunction and flatfoot: analysis with simulated walking. Gait Posture. 2013; 37(2): 264–268.
- Yoshida Y, Marcus RL, Lastayo PC. Intramuscular adipose tissue and central activation in older adults. Muscle Nerve. 2012; 46(5): 813–816.
- Yu TY, Pang JHS, Wu KPH, et al. Aging is associated with increased activities of matrix metalloproteinase-2 and -9 in tenocytes. BMC Musculoskelet Disord. 2013; 14: 2.
